Fertilizer-Derived Uranium and its Threat to Human HealthEwald Schnug†,* and Bernd G. Lottermoser‡

† Fakultat fur Lebenswissenschaften der Technischen Universitat Braunschweig, Pockelsstraße 14, D-38106 Braunschweig, Germany‡ Environment and Sustainability Institute, University of Exeter, Cornwall Campus, Penryn, Cornwall, TR10 9EZ, U.K.

Phosphate fertilization remains the main source of uraniumcontamination of agricultural land, primarily due to

impurities in the phosphate rock used for fertilizer manufacture.In particular, long-term application of uranium-bearingfertilizers can significantly elevate the uranium concentrationin fertilized soils. The magnitude of uranium enrichment ofcultivated soils varies, depending on phosphate fertilizerapplication rate, uranium content of applied fertilizer, soiltype and prevailing climate. In Germany, the use of phosphatefertilizer from 1951 to 2011 has resulted in a cumulativeapplication of approximately 14 000 t of uranium onagricultural land, corresponding to an average cumulativeloading of 1 kg of uranium per hectare.1

Fertilizer-derived uranium in soils is prone to leachingbecause uranium is mobile in surface soils as uranyl complexdepending on prevailing pH and Eh conditions. Alternatively,uranium can be immobilized in subsurface materials by sorptionor coprecipitation mechanisms. The fate of uranium in soil andsubsurface environment is therefore influenced by a delicatebalance of U6+ association between immobile and mobilephases. Yet, uranium is highly soluble as uranyl (U6+) complexunder oxidizing conditions. Consequently, mobility of fertilizer-derived uranium from agricultural soils into ground and surfacewaters has been recognized in agricultural catchments and,numerous studies have established the transfer of fertilizer-derived uranium from soils into ground, surface and marinecoastal waters. For example in Germany, rivers and streams ofagricultural catchments have 10 times higher uraniumconcentrations (0.08 versus 0.8 μg/L U) than those dominatedby forestry.1 Significantly enriched uranium concentrations (>2μg/L U) were detected in heavily cultivated catchments.

Moreover, unconfined aquifers below agricultural land, ground-water has 3 to 17 times higher uranium concentrations thanthat below forested regions. Generally, there is a concurrentand strong correlation of dissolved uranium concentrations ingroundwater with those of other highly mobile and fertilizer-derived elements such as boron, magnesium, and potassium aswell as nitrate.1 The likely reason for the strong uranium-nitratecorrelation in groundwater could be due to (a) increasedfertilization of agricultural land using NP and NPK fertilizers;(b) significant mobility of fertilizer-derived uranium as uranyl-carbonate complex and transfer into the underlying aquifer; and(c) pronounced solubility of uranium as uranyl−nitratecomplex into groundwater. In northern Germany, unmineral-ized groundwater used as drinking water supply containsvariable uranium contents, with one-quarter to two-thirds likelyimpacted by fertilizer-derived uranium.1 Thus, agricultural soilsand nearby land and water resources are becoming increasinglycontaminated by uranium due to fertilizer use. Fertilizer-deriveduranium has entered German drinking water supplies.Principal route of exposure of humans to uranium occurs via

ingestion, skin contact, and inhalation. In particular, naturallymineralized groundwaters and bottled mineral waters cancontribute significantly to uranium uptake. In Germany, morethan 2 million people currently receive drinking water thatcontains >10 μg/L uranium. Here, a carnivore with a skewedtaste for offal, shellfish, and bottled mineral water can achievethe highest uranium uptake.1

A considerable body of evidence suggests that overexposureto uranium in drinking water may cause significant healtheffects in both humans and animals. Reported health effects ofuranium derive from experimental animal studies and humanepidemiology. Uranium may damage biological systemsthrough its chemical toxicity as well as its radioactivity, withthe chemical toxicity perceived as the primary health hazard andthe effects from uranium’s ionizing radiation being of secondaryconcern. The main health concerns with respect to uranium arerenal, developmental, reproductive, diminished bone growth, aswell as DNA and brain damage.2 In humans uranium isparticularly known for its nephrotoxic nature, with short-termand long-term exposure to uranium through drinking waterleading to renal effects. The information available on thechronic health effects caused by the exposure to uranium indrinking water points to the fact that regions with elevatedgroundwater uranium concentrations and more groundwateruse have an increased incidence of certain diseases. Forexample, increasing incidence in chronic kidney disease in SriLankan nationals has been related to the low-level fertilizer-

Received: January 16, 2013Accepted: January 29, 2013Published: February 27, 2013

Viewpoint

pubs.acs.org/est

© 2013 American Chemical Society 2433 dx.doi.org/10.1021/es4002357 | Environ. Sci. Technol. 2013, 47, 2433−2434

derived uranium contamination of groundwater that is used asdrinking water supply.3 Also, greater consumption of ground-water with higher uranium concentrations leads to a greater riskin humans in South Carolina to develop a range of cancertypes.4 Furthermore, uranium is an endocrine-disruptingchemical, leading to an increased risk of fertility problemsand reproductive cancers in animals when exposed to drinkingwater that contains uranium below the WHO and U.S. EPAwater standard (30 μg/L).5 Clearly, further research is neededon the long-term exposure of humans to low-level uraniumconcentrations at or below water quality guidelines. Populationsexposed to drinking water supplies contaminated with fertilizer-derived uranium should be followed for their increased risks ofdevelopmental defects and health effects.Present research efforts must focus on understanding the

source-pathway-receptor chains of fertilizer-derived uranium.Concurrently, the exposure of humans to this pollutant shouldbe limited. Such reduced exposure can be achieved throughuranium extraction during phosphoric acid manufacturing. Thisin turn would lead to an important supply of uranium fuel fornuclear power plants as well as reduced contaminant loadingsof agricultural soils and limited transfers of a pollutant into thehuman food chain.

■ AUTHOR INFORMATIONCorresponding Author*Phone: +49 173 2367829; e-mail: e.schnug@tu-braunschweig.de.NotesThe authors declare no competing financial interest.

■ REFERENCES(1) Schnug, E. Uran in Phosphor-Dungemitteln und dessen Verbleibin der Umwelt. Strahlentelex 2012, 612−613, 3−10 (in German).(2) Brugge, D.; Buchner, V. Health effects of uranium: New researchfindings. Rev. Environ. Health 2011, 26, 231−249.(3) Chandrajith, R.; Seneviratna, S.; Wickramaarachchi, K.;Attanayake, T.; Aturaliya, T. N. C.; Dissanayake, C. B. Naturalradionuclides and trace elements in rice field soils in relation tofertilizer application: Study of a chronic kidney disease area in SriLanka. Environ. Earth Sci. 2010, 60, 193−201.(4) Wagner, S. E.; Burch, J. B.; Bottai, M.; Puett, R.; Porter, D.;Bolick-Aldrich, S.; Temples, T.; Wilkerson, R. C.; Vena, J. E.; Hebert,J. R. Groundwater uranium and cancer incidence in South Carolina.Cancer, Causes Control 2011, 22, 41−50.(5) Raymond-Wish, S.; Mayer, L. P.; O’Neal, T.; Martinez, A.;Sellers, M. A.; Christian, P. J.; Marion, S. L.; Begay, C.; Propper, C. R.;Hoyer, P. B.; Dyer, C. A. Drinking water with uranium below the U.S.EPA water standard causes oestrogen receptor-dependent responses infemale mice. Environ. Health Perspect. 2007, 115, 1711−1716.

Environmental Science & Technology Viewpoint

dx.doi.org/10.1021/es4002357 | Environ. Sci. Technol. 2013, 47, 2433−24342434